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. Author manuscript; available in PMC: 2008 Dec 31.
Published in final edited form as: Anat Rec A Discov Mol Cell Evol Biol. 2006 Dec;288(12):1243–1249. doi: 10.1002/ar.a.20396

Remodeling dynamics in the Alveolar Process in Skeletally Mature Dogs

Sarandeep S Huja 1,*, Soledad A Fernandez 2, Kara J Hill 1, Yan Li 2
PMCID: PMC2612758  NIHMSID: NIHMS68680  PMID: 17075846

Abstract

Bone turnover rates can be altered by metabolic and mechanical demands. Due to the difference in the pattern of loading, we hypothesized that there are differences in bone remodeling rates between the maxillary and mandibular alveolar processes. Furthermore, in a canine model, the alveolar process of teeth that lack contact (e.g., 2nd premolars) would have a different turnover rate than bone supporting teeth with functional contact (e.g., 1st molars). Six skeletally mature male dogs were given a pair of calcein labels. After sacrifice, specimens representing the anterior and posterior locations of both jaws were prepared for examination by histomorphometric methods to evaluate the bone volume/total volume (BV/TV, %), bone volume (BV, sq. mm), mineral apposition rate (MAR, µm/d.) and bone formation rate (BFR, %/yr.) in the alveolar process. There were no significant differences (p > 0.05) in the BV/TV within the jaws. The bone volume within the alveolar process of the mandible was 2.8 fold greater than in the maxilla. The MAR was not significantly different between the jaws and antero-posterior locations. However, the BFR was significantly (p < 0.0001) greater in the mandible than in the maxilla. The anterior location had higher (p = 0.002) remodeling than the posterior location in the maxilla but not in the mandible. While there was a greater bone mass and increased remodeling in the mandible, no remodeling gradient in the coronal-apical direction was apparent in the alveolar process. Bone adaptation probably involves a complex interplay of bone turnover, mass and architecture.

Keywords: Bone, remodeling, adaptation, histomorphometry, alveolar process

INTRODUCTION

Remodeling is a primary homeostatic and healing mechanism in osseous tissues. Alteration in bone turnover occurs in disease (Parfitt, 1988; Boivin and Meunier, 2002) and also can be ascribed to physical forces (Carter, 1984; Daegling and Hotzman, 2003). Because bone remodeling serves a distinct purpose (Burr, 1993), researchers have sought to understand variations and mechanisms responsible for bone turnover in the axial and appendicular skeleton. Bone turnover in the alveolar process is important for understanding orthodontic tooth movement, tooth loss associated with aging periodontal disease and osteonecrosis of the mandible. There is preliminary evidence to suggest that bone turnover is 10 fold greater in the mandibular alveolar process of certain teeth than in the mid shaft of the tibia in a canine model (Tricker et al., 2002). Also, two other important observations regarding remodeling in the alveolar process of dogs have been made. First, bone turnover in the alveolar process of aged (10–12 yr.) dentate dogs from the mandibular 3rd premolar region is lower than similar regions in younger animals (Dixon et al., 1997). Secondly, bisphosphonates decrease bone turnover in the alveolar process but alveolar remodeling rate still remains higher than compared to other appendicular skeletal sites (Handick, 2001). It is possible that a local mechanism is responsible for the bone remodeling in the alveolar process. As the teeth are loaded intermittently during biting, and engineering strains have been measured on bone surface in jaws (Kakudo et al., 1973; Judge et al., 2003) it is likely that the alveolar process receives strains during physiologic functions. It is important to connect the biological reactions/response to mechanical loading in the craniofacial skeleton. For example, understanding the role of biting forces (Fontijin-Tekamp et al., 1998), engineering strains (Ravosa et al., 2000) and biologic adaptation is important to bone biologist and clinicians.

The focus of this research is to understand the pattern of bone turnover in the alveolar process. We hypothesize that differences in bone turnover exists a) within the alveolar process b) between jaws and c) between anterior and posterior locations, in a canine model. If differences existed it may suggest that a certain site may adapt to components of physical forces by altering remodeling rates. This mechanical environment then would be a candidate for further investigation.

METHODS AND MATERIALS

ILACUC approval was obtained for the study and six mature male beagle dogs were maintained in The Ohio State University Animal Facility for this study. For the ~ 3 week duration of this experiment, the animals were fed standard dry dog chow and water ad libitum. The dogs were monitored for normal behavior and weight maintenance. Intravital calcein bone labels (Sigma, St. Louis, MO, 5mg/kg) to mark forming bone surfaces were administered 16 and 2 days prior to sacrifice. Each animal was euthanized using pentobarbital (IV), a method recommended by the AVMA Panel on Euthanasia.

Alveolar bone specimens (n=48) were obtained from six, 1–2 year old skeletally mature male dogs. Eight specimens representing the anterior and posterior locations within the maxilla and mandible were obtained from each dog. Each specimen consisted of a section through the jaw containing the tooth and its surrounding alveolar process. Anterior specimens were obtained bilaterally from the mesial root of the maxillary and mandibular permanent second premolars (P2). Maxillary posterior specimens were obtained bilaterally from the distal root of the maxillary permanent 4th premolar (P4) and the mandibular posterior specimens consisted of the alveolar process of the distal root of the permanent first molars (M1) region. Bone sections were made bucco-lingually, through the center of the longitudinal axis of a tooth root using a saw (Exakt 310 CP, Exakt Technologies, Oklahoma City, OK) under water lubrication. The undecalcified, unstained specimens were embedded in resin and then cut/ground (~80–100 µm thickness) using standard histological techniques (Donath and Breuner, 1982).

The study was blinded to conceal the identification of the specimen under examination. Each section was examined under epifluorescence (Olympus, BX 51, Tokyo, Japan) at 100X at optimal wavelengths. Static and dynamic histomorphometric parameters, using standard hit/intercept methods with aid of a Merz grid, were evaluated (Parfitt, 1983). All measurements were made by one examiner. Intra examiner variability, measured by examining 4 sections, 2 weeks apart was ~ 4–5% for the histomorphometric variables examined. The Merz grid was placed over the bone on the buccal alveolar crest region (Fig. 1) and the raw data to calculate the variables of interest were collected. The Merz grid was then moved apically and eventually data to cover the entire alveolar process to the level of the root tip on the buccal side were collected. Typically ~11–15 grids at 100X were sufficient to analyze the entire buccal alveolar process. Similarly alveolar bone data for the lingual/palatal side of the tooth were collected. On the palate, the data were acquired for a distance of 1 mm from the periodontal ligament. This distinction is required, as the alveolar process blends with the palate in the maxilla and the boundary between alveolar process and palatal bone does not exist. From these measurements, the following histomorphometric variables (Parfitt et al., 1987) were calculated: bone volume/total volume (BV/TV, % - bone hits/total hits*100), mineral apposition rate (MAR, µm/d - interlabel width/number of days), bone formation rate (BFR, %/yr. - MAR * (DL int. + 1/2 SL int. ) /BV) * 100* 365). In addition, we calculated bone volume (BV, sq. mm – (bone hits)2) to understand the bone mass contained within the alveolar process. We have reported BFR in %/yr. to allow for comparisons with other studies. For each dog, 2 cross sections of the left femoral mid-diaphyses were also analyzed by histomorphometry. This is an important internal comparison as variations in cortical bone turnover from 2 – 10 %/year have been reported (Burr, 1993). In addition, abnormal femoral BFR values may indicate bone pathology. After the data were collected, the alveolar process on the buccal and lingual/palatal side was divided into thirds (coronal, middle, apical-regions), based on the distance from the alveolar crest to root tip (Fig. 1) for further analyses.

Fig. 1.

Fig. 1

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Schematic of alveolar process and method for collection of histomorphometric data. Merz grid is represented by square on alveolar process. The entire alveolar bone from buccal/lingual/palatal crest to the root apex was sampled. After the data was collected, the alveolar process was divided into thirds (1-coronal, 2-middle, 3-apical). Only bone within the alveolar process is included in the measurements, certain parts of the Merz grid will extend beyond the alveolar bone.

Statistical analyses

Linear mixed models with repeated measures were used to study the effect of region, jaw and location on the 4 outcome variables BV, BV/TV, MAR and BFR. The data consist of repeated measures taken on the same tooth for the 6 different regions. Region, jaw, location as well as the significant interaction terms between each of these factors were included as fixed effects in these models. In order to simplify model interpretations, interactions were only included if significance was found at the alpha level of 0.01. Random intercepts were included in all models. The autoregressive with lag = 1 structure was used for random effect and the repeated measurement components for this study. We assumed that the correlation between two regions would decrease as the distance between the two locations increased.

RESULTS

Means and standard deviations for each (a) region of both jaws and (b) anterior-posterior location for each jaw, for the histomorphometric variables of interest are presented (Table 1). Statistical differences from the mixed model analyses of the histomorphometric parameters and significant interaction terms are presented in Table 2.

Table 1a.

Descriptive statistics represented by the Means and SD of histomorphometric variables for (a) each jaw and region (b) each jaw and location (anterior and posterior). BV = Bone Volume, MAR = Mineral Apposition Rate, BFR = Bone formation rate and BV/TV = Bone volume/total volume. In Table 1a, the values represent the means for both the anterior and posterior teeth combined for each region. In Table 1b, the values at each location represent the combination of all 6 regions.

BV (sq. mm) BV/TV % MAR (µm/d.) BFR (%/yr.)
JAW REGION Mean SD Mean SD Mean SD Mean SD
Maxilla 1 0.7 0.4 99.9 0.2 1.3 0.6 11.6 17.6
2 1.3 0.8 98.3 2.7 1.6 0.3 18.7 21.7
3 1.9 0.8 97.1 4.4 1.6 0.4 17.1 16.0
4 2.2 0.9 97.6 2.7 1.6 0.2 22.8 21.7
5 2.8 0.9 97.8 2.0 1.5 0.4 23.4 16.4
6 1.5 1.0 98.4 2.3 1.5 0.3 22.2 16.8
Mandible 1 2.3 1.3 97.7 3.6 1.5 0.3 42.8 34.0
2 3.7 1.7 98.0 2.3 1.6 0.2 35.8 19.5
3 4.8 2.4 98.1 2.0 1.6 0.3 36.7 26.3
4 7.0 3.3 97.6 1.6 1.6 0.2 27.5 13.0
5 6.4 3.1 97.5 1.8 1.5 0.2 31.6 19.7
6 4.0 1.9 97.9 1.5 1.6 0.2 46.9 24.5
Table 1b
JAW LOCATION Mean SD Mean SD Mean SD Mean SD
Maxilla Anterior 10.4 2.7 97.5 3.3 1.5 0.3 26.6 20.8
Posterior 10.2 3.5 98.9 2.0 1.6 0.4 11.7 12.4
Mandible Anterior 19.6 7.5 97.8 2.1 1.5 0.2 36.1 27.2
Posterior 36.5 7.5 97.9 2.3 1.5 0.2 37.7 21.0
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Table 2.

Significant main effects and interactions obtained from the mixed model analyses for the histomorphometric variables. Interactions at the p ≤ 0.01 level were considered significant. BV = Bone Volume, MAR = Mineral Apposition Rate, BFR = Bone formation rate and BV/TV = Bone volume/total volume.

Variable Comparison P value
BV Main Effects
   Jaw: Maxilla vs. Mandible < 0.0001
   Location: Anterior vs. Posterior <0.0001
Interaction
   Jaw*Location <0.0001
BV/TV Main Effects
   Location: Anterior vs. Posterior 0.049
MAR Main Effects
   Region 0.035
BFR Main Effects
   Jaw: Maxilla vs. Mandible <0.0001
   Location: Anterior vs. Posterior 0.028
   Region 0.20
Interaction
   Region*Jaw 0.003
   Jaw*Location 0.006
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Static measurements

Bone Volume (BV, sq. mm)

This parameter reflects the entire bone mass or area of the alveolar process supporting the teeth examined. This includes the bone from the level of the alveolar crest to the apex of the tooth root. The terminology (BV) is consistent with the nomenclature suggested in the literature (Parfitt et al., 1987). There was a significant difference between jaws (p < 0.0001) and antero-posterior location (p < 0.0001) for BV. However, there were significant interactions of jaw and location (Table 2). A ~ 2.8 fold greater mean BV existed in the alveolar process in the mandible as compared to the maxilla. The posterior teeth for both jaws combined, had 1.5 fold greater bone support than the anterior teeth. However, due to the interactions, when separated by jaw the results were different. There was a 2 fold difference (p < 0.0001) in alveolar process area when the mandibular posterior teeth were compared to the mandibular anterior teeth. In the maxilla the bone supporting the maxillary anterior location had similar (p = 0.84) BV to the posterior location (Table 1b).

Bone Volume/Total Volume (BV/TV, %)

BV/TV % is a reflection of the density or lack of porosity of the bone. The mean BV/TV was 98.2% in the maxillary alveolar process and 97.8% in the mandibular alveolar process but they were not significantly different. Also, the posterior teeth had a significantly (p = 0.049) greater mean BV/TV of 98.3 % (SE = 0.4) compared to the 97.7% (SE = 0.4) of the anterior teeth.

Dynamic Measurements

Mineral Apposition Rate (MAR, µm/day)

This parameter reflects the tissue level activity of the bone cells. The MAR in the jaws was 1.5 (SE = 0.3) µm/d. compared to 1.3 (SE = 0.2) µm/d. in the femur. No difference was shown to exist between jaw (p = 0.6) and antero-posterior location (p = 0.7) for MAR. There were overall regional differences (p < 0.035) in MAR, with a trend towards the most coronal regions having lower MAR than the middle and apical regions. In contrast, there was no significant difference (p = 0.13) in MAR between the middle and apical regions.

Bone Formation Rate (BFR, %/yr)

This parameter is a product of the rate of mineral apposition and the number of sites of bone formation within a specified bone volume. First, there were no significant regional (coronal, middle, apical) differences (p = 0.2) in the BFR. However, there were significant difference (p < 0.0001) between the maxilla (19.1%/yr; SE = 4.3) and mandible (36.9%/yr; SE = 4.3). In addition for both jaws combined, the anterior teeth (31.3%/yr.; SE = 4.3) had a significantly higher (p = 0.03) remodeling than the posterior teeth (24.7%/yr; SE = 4.3). When the antero-posterior locations were examined within a jaw, the BFR within the mandible was similar for the anterior and posterior tooth supporting bone (Table 1b) but in the maxilla the BFR was 2 fold greater in the anterior region than in the posterior regions. The mean BFR in the mid femoral diaphyses of the 6 dogs was 6.4%/yr. (SE = 4.3).

DISCUSSION

This study describes bone turnover in the alveolar process. In addition, we attempted to isolate areas of altered turnover with the future objective of examining difference in mechanical loading. Under physiologic conditions we found a variation in bone turnover a) between jaws and b) between anterior and posterior tooth supporting bone, in a canine model. We did not find regional differences or a coronal-apical graident in rate of turnover within the alveolar process. However, it is clear that alveolar turnover rate was 3–6 fold higher than the femur.

The rationale for examining anterior versus posterior teeth in dogs is based on the functional anatomy. Unlike humans, in dogs the second premolars are not in occlusion (Miller et al., 1964). However, the maxillary 4th premolars and mandibular first molars are the shearing teeth in dogs (Bryant and Russell, 1995). In this study, we have not measured the bite forces on the anterior versus the posterior teeth. Neither do we have details on the masticatory cycle of these purpose bred dogs. It is known that the microanatomy and bone formation dynamics of bone support in erupting teeth and teeth with aging are different (Anderson and Danylchuk, 1979a; Von Wowern and Stoltze, 1980; Jager, 1996) from adult alveolar process. Bone adaptation involves changes in bone mass, architecture and material properties. The interplay between these factors may be more apparent if the mechanical and metabolic environment were known at each sequential time points along the dog’s life. Thus, a limitation of this study is that we are examining the remodeling dynamics at a single time point (age of dog). Another reason for examining remodeling is the differences in the mechanical environment between the maxilla and mandible. Strain gauge and experimental data suggest that the mandible of monkeys and humans is exposed to torsional forces (Hylander and Crompton, 1986; Daegling and Hylander, 2000; Ravosa et al., 2000). However the thin maxillary bone is suggested to resist compressive force of mastication. Isolation of individual components of force (e.g., shear vs. tension) and their relation to remodeling while interesting is extremely complex.

We made measurements within the alveolar process of each jaw. While it is generally agreed that the maxilla is a more porous bone than the mandible, the < 1% difference in BV/TV% not likely to be biologically significant. We ascribe the relative smaller BV/TV% in the mandible to the higher rate of bone remodeling. This increased porosity could easily be accommodated by the increase in bone mass in the mandible. It is not clearly understood what controls the bone mass of the alveolar process. However, the alveolar process in the maxilla (Fig. 2a) is extremely thin. In contrast the mandibular alveolar process is thicker (Fig. 2b). It is possible that the thickness of the alveolar process is not related to biting forces per se, but the reaction of the bite forces produce within the jaw that the teeth are contained. Also, there was no significant difference in the mandible in the BFR for the anterior vs. the posterior location, even though physiological differences in tooth contact exist in these two regions. However, in the maxilla the anterior region had a 2 fold greater remodeling rate, even thought the bone mass of the maxillary P2’s were not different from the P4. As no difference was shown to exist in BV but a difference exists in the remodeling rate in the anterior and posterior location of the maxilla, an examination of the strains on the surface and within the bone of these regions may provide information on the loading environment.

Fig. 2.

Fig. 2

Fig. 2

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Composite epifluorescent photomicrographs of a representative (a) Maxillary left 4th premolar and (b) Mandibular right 2nd premolar. Multiple images were stitched to make the entire composite. Each individual image was taken at 100X as epifluorescense is not clearly seen at low magnification that would be needed to obtain a photomicrograph of an entire tooth and supporting alveolar bone. The maxillary tooth ( B is buccal, and P is palatal) has a very thin alveolar process. Bone remodeling is seen by the presence of single and double calcein bone labels in the mandibular alveolar process (B is buccal and L is lingual) and body of mandible.

The remodeling dynamics of the appendicular skeleton in dogs is well characterized (Harris et al., 1968). Unlike mice or rats, dogs and non-human primates are good models to study osteonal remodeling. However, there is still very limited published information on the osteonal remodeling process in the alveolar process. In addition, very few studies examine dynamic histomorphometric parameters by the double labeling technique. These paired labels are required to assess MAR and BFR and for quantitative analyses. A static approach to quantify tissue bone level activity involves measurement of osteoid seams with or without osteoblasts and resorption surfaces with and without osteoclasts (Jager, 1996). Such studies provide information in anabolic and catabolic activity within a tissue specimen and have been reported for alveolar process in humans (Devlin et al., 1994; Jager, 1996; Verna et al., 1999) and monkeys (Melsen, 1999). This histologic method does not require the administration of fluorescent bone labels and is a reflection but not a direct measure of osteonal remodeling rate. However, this static method can be advantageous as measurements can be made from cadaveric specimens. Studies suggest that approximately 15–20% of the bone of the alveolar process is covered with osteoid and approximately 3–7% is undergoing resorption in teeth not subjected to orthodontic forces (Jager, 1996; Melsen, 1999).

In one previous study, turnover dynamics were measured in the alveolar process surrounding the third permanent premolars in the mandible of 1–2 yr old dogs (Tricker et al., 2002). Corono-apically, a decreasing gradient of bone turnover, with a range for BFR of 37.3 – 15.3%/yr. was recorded in the mandible. In the alveolar process the BFR had a range of 21.9–37.3%/yr. The lower value of 15.3% was indicative of the turnover in the base of the mandible, away from the alveolar process. Our values for MAR and BFR are remarkably similar to the above study in the mandible, considering they were done on entirely different dogs and on different teeth.

One study, published in the Italian literature can be compared to our study (Marotti and De Lena, 1966). Mogrel dogs (age range 4 m to 6 yr.) received Ledermycin to mark bone formation. Multiple sections were made both to include the roots of mandibular teeth and interradicular regions. This study confirmed that the qualitative rate of turnover was greater in the anterior (canine-1st premolar) and posterior (ramus) regions of the mandible when compared to the 4th premolar and 1st molar region. Also, they stated that more bone label was seen in the alveolar process than the body of the mandible. They also pointed out an age effect, with older dogs having a lower turnover than the younger age group.

The MAR values recorded in this study are consistent with the literature for dogs (Anderson and Danylchuk, 1979b; Wronski et al., 1981). The turnover in the alveolar process of the maxilla and mandible are 3 and 6 fold higher respectively, than the femur. The reason of this turnover is not clearly understood. Given this turnover is occurring in the small volume of tissue (~10 mm2 in maxilla vs. ~ 28 mm2 in mandible), this constitutes an elevated localized remodeling response. It can be hypothesized that the remodeling attempts to decrease the localized tissue age, and thus lowers the material properties of the tissue. This would result in a more compliant bone, capable of bending without accumulating microdamage. One would then expect that if the remodeling rate was lowered (for example with bisphosphonates), microdamage would accumulate. If microdamage does not accumulate (Engen, 2002), then the alternate hypothesis could be that linear microdamage and fatigue based mechanism is probably not likely in the alveolar process. However, it has been suggested that repair of microdamage maybe one reason for the elevated turnover (Verna et al., 2004; Verna et al., 2005) subsequent to orthodontic tooth movement. The amount of microdamage present in the non-orthodontic samples (Engen, 2002; Verna et al., 2004; Verna et al., 2005) is substantially lower than that would clearly account for targeted remodeling (Parfitt, 2002) being the only mechanism within the alveolar process. It is possible that a certain percentage of the total remodeling is stochastic (Burr, 2002). It is well known that bone turnover, at a cell level, maybe controlled by biophysical signals and they could play a role in determining bone turnover.

It is intriguing that the remodeling rate in the alveolar process in the maxilla and mandible is elevated by 3 to 6 fold of when compared to femoral sites. Presence of tooth contact does not solely explain the altered remodeling rate. At a tissue level, bone adaptation in the alveolar process probably involves a complex interplay of bone turnover, mass and architecture. The stimulus and mechanism for this elevated turnover should have considerable implications for clinicians and bone biologists.

ACKNOWLEDGMENTS

Funding from NIDCR Grant R03 DE015233 is acknowledged.

Grant Sponsor: NIDCR Grant Number: R03 DE015233

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